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Ophthalmology. Author manuscript; available in PMC 2012 October 1.
The Joint Writing Committee for the Multi-Ethnic Pediatric Eye Disease Study and the
Baltimore Pediatric Eye Disease Study Groups*, Mark Borchert, Rohit Varma, Susan
Cotter, Kristina Tarczy-Hornoch, Roberta McKean-Cowdin, Jesse Lin, Ge Wen, Jolyn Wei,
Stan Azen, Mina Torres, James M. Tielsch, David S. Friedman, Michael X. Repka, Joanne
Katz, Lydia Giordano, and Josephine Ibironke
Doheny Eye Institute and the Department of Ophthalmology, Keck School of Medicine, University
of Southern California, Los Angeles, California; Department of Preventive Medicine, Keck School
of Medicine, University of Southern California, Los Angeles, California; Division of
Ophthalmology, Childrens Hospital Los Angeles, Los Angeles, California; Dana Center for
Prevention Ophthalmology, Wilmer Eye Institute, The Johns Hopkins University School of
Medicine, Baltimore, Maryland; Department of International Health, the Johns Hopkins Bloomberg
School of Public Health, Baltimore, Maryland; Zanvyl Krieger Children's Eye Center and Adult
Strabismus Service, Wilmer Eye Institute, The Johns Hopkins University School of Medicine,
Baltimore, Maryland; Department of Pediatrics, The Johns Hopkins University School of
Medicine, Baltimore, Maryland
Abstract
PurposeTo describe the risk factors associated with hyperopia and myopia among children
aged 6 to 72 months.
DesignPopulation-based cross-sectional study.
ParticipantsPopulation-based samples of 9970 children ages 6 to 72 months from Los
Angeles County, California, and Baltimore, Maryland.
2011 American Academy of Ophthalmology, Inc. Published by Elsevier Inc. All rights reserved.
Correspondence: Rohit Varma, MD, MPH, Doheny Eye Institute, Department of Ophthalmology, 1450 San Pablo St., Room 4900,
Los Angeles, CA 90033. Phone: (323) 442-6411, FAX: (323) 442-6412, rvarma@usc.edu.
*See Appendix 1 (available at http://aaojournal.org) for members/affiliations of the MEPEDS and BPEDS Groups.
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our
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Conflicts of Interest: The authors have no proprietary or commercial interest in any materials discussed in the manuscript.
et al.
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Methods
The protocol and informed consent forms were reviewed and approved by the Institutional
Review Board (IRB)/Ethics Committee of the Los Angeles County/University of Southern
California Medical Center, the Committee on Human Subjects Research at the Johns
Hopkins Bloomberg School of Public Health, the Battelle Centers for Public Health
Research and Evaluation IRB, and the IRB of the Maryland Department of Health and
Mental Hygiene, and complied with current Health Insurance Portability and Accountability
Act regulations. A parent or guardian of each study participant gave written informed
consent. An independent data monitoring and oversight committee provided study oversight.
Study Cohort
The study population, consisting of children aged 6 to 72 months, was identified by door-todoor screening of families within 74 census tracts in and around the cities of Inglewood,
Riverside, and Glendale, California, for MEPEDS, and from 54 census tracts in and around
the city of Baltimore, Maryland, for BPEDS. The details of the screening process have been
reported elsewhere.11, 14 After written informed consent was obtained, an appointment was
scheduled for a comprehensive eye examination in either the local study center or a bus
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Page 3
outfitted for mobile eye examinations. In Maryland, examinations were performed in the
homes of families unable to travel to the study center.
The analysis cohort consisted of all children in whom reliable cycloplegic refraction could
be obtained. Spherical equivalent (SE) refractive errors from the right eye of each
participant were used for purposes of this report. Myopia was defined as SE refractive error
1.00 diopter; hyperopia as SE refractive error +2.00 diopters. Based on previously
published reports and consensus of all the investigators, the lowest levels of ametropia
considered to meet the definition of myopia or hyperopia in preschoolers are presented. Risk
factors for these outcomes were explored using univariate analysis and multiple logistic
regression analysis. Demographic and socioeconomic factors evaluated included study site
(California or Maryland); age; sex; ethnic group (Hispanic white; non-Hispanic white;
African-American; determined by parental report); household annual income (<$20,000;
$20,000); regular primary care (last checkup within past 2 years or not); self-reported
difficulty accessing care (yes or no); health insurance (yes or no); vision insurance (yes or
no); education of primary and secondary caregivers (completed or not completed high
school) and preschool or daycare attendance (yes or no; MEPEDS only). Behavioral and
clinical risk factors evaluated for both outcomes included maternal smoking during
pregnancy (yes or no); pack-months of maternal smoking during pregnancy; maternal
alcohol consumption during pregnancy (yes or no); maternal age at birth of child (<35 years;
35 years); gestational age (<33 weeks; 33 weeks); low birth weight for gestational age15
(yes or no); breastfeeding (yes or no); family history of strabismus or amblyopia in first
degree relatives (yes or no); Down syndrome (yes or no); and cerebral palsy (yes or no).
Finally, the association of astigmatism 1.50 diopters in any axis of the right eye with
hyperopia or myopia was explored.
Univariate chi-square or, where appropriate, Fishers exact tests were first performed for all
of these demographic, behavioral, and clinical risk factors. Variables showing at least
marginally significant associations (P<0.1) in univariate analyses were considered
candidates for subsequent forward stepwise multiple logistic regression, with the exception
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of Down syndrome and cerebral palsy, which were excluded from multivariate models due
to the very small numbers of children with these conditions. LOWESS plots (locally
weighted polynomial regression) were created to examine the independent relationship
between a given continuous risk factor and the prevalence of an outcome. Regression
models were fitted conditioned on the continuous variable and adjusted for all other
variables significantly associated with the outcome. The estimated prevalence of the
outcome was plotted against the continuous variable. The LOWESS plot uses an iterative,
locally weighted, least-squares method to plot the best-fit line (STATA). (Cleveland and
Devlin 1988) 16
Individuals with missing data were excluded from the univariate analysis for that variable;
multivariate models were run first restricted to those with complete data for all variables
entered into the model and re-run in the final analysis for all individuals with complete data
for variables selected in the final step-wise regression. Formal tests of interaction were
completed by including a product term in the multivariate model for maternal prenatal
smoking with age, gender, and race/ethnicity. Odds ratios (OR) with 95% confidence
intervals (CI) are reported for the significant independent risk factors included in the final
model
Results
Eighty percent of eligible MEPEDS children and 62% of eligible BPEDS children were
examined. Comparison of participants and nonparticipants is published elsewhere.14,17
Refractive error was determined with cycloplegia in nearly all participants. As previously
reported, only 4.7% of BPEDS participants and 4.1% of MEPEDS participants underwent
non-cycloplegic retinoscopy due to parental refusal of eyedrops.18 Spherical equivalent
refractive error of the right eye could not be determined in 77 of the 9869 children who met
race/ethnicity inclusion criteria (Fig 1). Testability of refractive error using the retinomax
auto-refractor as a function of age has been previously reported.19
et al.
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factors were unchanged if myopia was redefined as 0.5 diopter. When myopia was
defined as 2.00 diopters, age group lost significance, but limited access to health care
became an independent risk factor.
Hyperopia, on the other hand, is independently associated with astigmatism, and with
Hispanic and non-Hispanic white race/ethnicity (compared to African Americans), but does
not diminish with age (Table 3). It is, in fact, less prevalent in 1- to 3-year-olds, than in 6year-old children. Hyperopia is also associated with having health insurance and maternal
smoking during pregnancy. Astigmatism was not associated with hyperopia in those subjects
who were excluded from analysis for missing data. This was the only significant difference
in characteristics of children included in the data analysis compared to those excluded for
missing data.
Subgroup analysis showed that maternal smoking during pregnancy was a significant
independent risk factor for hyperopia only in the BPEDS cohort (OR= 1.70, 95% CI 1.33
2.18). The prevalence of maternal smoking during pregnancy in California was significantly
lower than in Maryland (5.3% vs. 20.5%), but maternal smoking during pregnancy remained
associated with hyperopia after adjusting for site (O.R. 1.43; 95% CI 1.201.70) and after
adjusting for site and race/ethnicity (O.R. 1.41; 1.181.69). The prevalence of missing
maternal smoking data was similar for the two locations (19% for California vs. 20%for
Maryland). Maternal smoking remained a significant risk factor for higher threshold levels
of hyperopia - hyperopia +3.00D (O.R. 1.45; 95% CI 1.141.84) and hyperopia +3.50D
(O.R. 1.39; 95% CI 1.021.90) for the entire cohort. There were no interactions of maternal
smoking with any other significant variable for hyperopia identified from the multivariate
model. There was no association of prenatal smoking with any level of myopia in both
univariate and multivariate analyses.
The association of hyperopia with pack-months of maternal smoking during pregnancy
exposure was also explored after adjusting for other significant risk factors determined by
the multivariate model. The relationship appears to be linear and dose-dependent, with a 6%
higher prevalence of hyperopia for every increase of 10 pack-months of maternal smoking
during pregnancy (Fig 2).
Discussion
Although major risk factors for myopia in school-age children are known to include family
history,21,22 environment,23 and ethnicity,24 less is known about the risk factors for
hyperopia. No previous population-based studies have addressed this issue in preschoolaged children. Using multivariate analysis in a population-based, multi-ethnic sample of
children, this study has identified risk factors associated with hyperopia and myopia in
children aged 6 to 72 months.
Notwithstanding the limitations of a cross-sectional study, the data presented here do not
support the notion of emmetropization in young children with hyperopia as the only
significant drop in the prevalence of hyperopia is at 1 year of age (p= 0.0001); and
hyperopia is less prevalent in 1- to 3-year-olds than in 6-year-olds (p=0.001). Conversely,
the prevalence of myopia is lower in children aged 46 years compared to those 3 years of
age and younger (p<0.0001). Previous papers by the BPEDS and MEPEDS groups also
showed minimal differences in the distribution of refractive errors by age in
preschoolers.18, 20 This again is in contradistinction to the higher prevalence of myopia and
lower prevalence of hyperopia noted in older school age children compared to younger
school aged children.25, 26 As this is not an incidence study, we cannot determine if subsets
of the ammetropic children are shifting toward or away from emmetropia. Nonetheless, the
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Page 6
increasing axial length associated with age during the first 5 years of life does not lead to
age-related shifts toward myopia in preschool children.27 Concomitant biometric changes in
the cornea or lens of young children would not be expected to be entirely spherical and
might explain independent association of astigmatism 1.50 diopters with both myopia and
hyperopia.
The results of this study cannot be directly applied to designing screening strategies in
preschoolers except to suggest that strategies based on detection of abnormal refractive
errors may be less age-dependent than previously thought. Since hyperopia +2.00 D is
associated with strabismus,12 yet is stable beyond 1 year of age, screening for hyperopia
may be initiated at any time beyond 1 year of age. This stability is similar to that previously
reported for spherical equivalent anisometropia 1.0 D beyond one year of age, which is
also associated with increased risk for amblyopia.13, 28 Thus, the age at which amblyopia or
strabismus develops as a result of ametropia or anisometropia may be an important
consideration in the timing of preschool screening programs that are based on refractive
errors. While our data provide some insights into the relationship between age, ethnicity,
refractive error and amblyopia and strabismus, caution must be exercised in interpreting our
data as they are cross sectional by design. Validation of these risk associations will require
further prospective research.
Race has a significant independent role in the risk of myopia and hyperopia, with AfricanAmerican and Hispanic children at significantly greater risk for myopia than non-Hispanic
whites and with African Americans at significantly less risk for hyperopia than Hispanics or
non-Hispanic whites. A previous population-based study of school-aged children also noted
that non-Hispanic whites were at significantly higher risk for hyperopia +2.00 D than
Asians or children of Middle Eastern descent.25 However, our study is the first comparing
risk factors for refractive error in non-Hispanic whites, Hispanics and African Americans.
Knowledge of age- and race-related relative risks for different refractive errors may impact
the screening strategies chosen for use in preschool children.
Maternal smoking during pregnancy is a significant independent and avoidable risk factor
for hyperopia in preschool age children, even after adjusting for the expected co-variables of
race, income, and education. This was similarly found to be the case in a population-based
study in Australia, though the association was found in 6-year-olds and was only borderline
in 12-year-olds.25 Another clinical study of parental smoking and refractive error in children
found parental smoking (one or both parents) was associated with a decreased risk of
myopia and an increased risk of hyperopia compared with children whose parents did not
smoke.29 In the same study, smoking by either parent during the pregnancy was associated
with decreased risk of myopia after adjusting for the childs age, body mass index, near
work, myopia status of parents, and parents education level. On the other hand, no
association between parental smoking and childhood myopia was found in a separate study
of children in Singapore.30
The strong association of maternal smoking with childhood hyperopia supports the notion
that nicotinic acetylcholine receptors may regulate eye growth in a manner antagonistic to
the muscarinic acetylcholine receptors that promote axial elongation of the eye.29 However,
nicotinic antagonists actually inhibit experimental myopia in chicks, making it unlikely that
nicotinic agonists found in tobacco do the same.31 Thus, the biological explanation for the
relationship of childhood hyperopia with smoking exposure remains speculative.
The independent association between being hyperopia and having health insurance status is
unlikely to be directly related. However, having health insurance may be a surrogate
et al.
Page 7
measure for unknown risk factors such as diet or type of prenatal care that were not
collected in our study.
Myopia was more likely in BPEDS participants than in MEPEDS participants in our
multivariate analysis, indicating an effect independent of race or ethnicity. This could reflect
genetic differences between similar racial populations in different geographical locations or
demographic or environmental differences that are not captured in the present analysis.
Since similarly small proportions of children were refracted without cycloplegia at the two
sites, the association with study site is unlikely to be an artifact of misclassification with
regard to refractive error.
The definitions of hyperopia (2 diopters) and myopia (1 diopter) could be questioned
since subjects with less severe refractive errors may still be considered to have the condition
and thus lead to misidentification of risk factors. When subjects with borderline refractive
error (hyperopia between 1 and 2 diopters or myopia between 0 and 1 diopter) were
excluded from the analyses, there was no change in the independent risk factors that were
identified.
Several limitations to this study are related to the cross-sectional study design. For example,
although the association of refractive error with age suggests loss of early myopia as
children age, longitudinal study is needed to confirm whether such a process of
emmetropization occurs. Since gestational exposure to maternal smoking was determined
retrospectively by parental report, there is the potential for recall bias, with parents of
children with refractive error being more likely to report such exposure. However, we
believe that such bias would be limited by the fact that refractive error was not measured
and communicated to parents until after completion of the parental interview.
Missing data may be another limitation of the study. We excluded 77 individuals because of
missing data from the myopia analysis and 1401 individuals from the hyperopia analysis;
however, we did not find significance differences in characteristics of participants included
in the analysis versus those who were excluded with the exception that a higher proportion
of those with astigmatism and hyperopia were included in the analysis.
The size and population-based design of this study are its major strengths. We believe our
results may be generalized to other similar populations and are less likely to be impacted by
referral or selection biases than findings from clinic-based studies. The use of identical
protocols in two sites has allowed us to pool MEPEDS and BPEDS data with resulting gains
in power and precision of our estimates of the strength of reported associations.
Supplementary Material
Refer to Web version on PubMed Central for supplementary material.
Acknowledgments
The MEPEDS-BPEDS Investigators would like to acknowledge the helpful advice and support of the members of
the National Eye Institute's Data Monitoring and Oversight Committee comprising of: Jonathan Holmes, MD
(Chair), Eileen Birch, PhD, Karen Cruickshanks, PhD, Natalie Kurinij, PhD, Maureen Maguire, PhD, Joseph
Miller, MD, MPH, Graham Quinn, MD, and Karla Zadnik, OD, PhD.
et al.
Page 8
Support: Supported by the National Eye Institute, National Institutes of Health, Bethesda, MD (grant nos.
EY14472, EY03040 and EY14483), and an unrestricted grant from the Research to Prevent Blindness, New York,
NY. Dr. Varma is a Research to Prevent Blindness Sybil B. Harrington Scholar.
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Figure 1.
Participant flowchart highlighting those children who were included and excluded from the
final analysis sample for both outcomes myopia and hyperopia in both the Multi-Ethnic
Pediatric Eye Disease Study and the Baltimore Pediatric Eye Disease Study.
et al.
Page 11
Locally weighted regression line illustrating the independent association of the amount of
maternal smoking during pregnancy and the estimated prevalence of hyperopia in both the
Multi-Ethnic Pediatric Eye Disease Study and the Baltimore Pediatric Eye Disease Study.
The estimated prevalence of hyperopia was obtained using a stepwise logistic regression
procedure that adjusts for other potential risk factors.
94 (6)
81 (4)
51 (3)
47 (3)
49 (3)
1223 Months
2435 Months
3647 Months
4859 Months
6072 Months
Breastfed
353 (96)
62 (4)
14 (4)
37 to <42 weeks
>= 42 weeks
26 (5)
297 (4)
33 to < 37 weeks
1589 (96)
547 (95)
7278 (96)
7 (3)
259 (97)
259 (97)
730 (96)
251 (95)
5636 (96)
20 to <33 weeks
Gestational age
4036 (94)
249 (6)
African-American
1082 (96)
3076 (97)
25 (1)
104 (3)
Hispanic White
2403 (99)
1801 (97)
1796 (97)
1774 (97)
1733 (96)
1596 (94)
815 (94)
2259 (95)
7256 (96)
No
N=9515
n (%)
Non-Hispanic White
Race
56 (6)
611 months
Age
269 (4)
Maryland
Yes
N=378
n (%)
California
Site
Myopia (-1D)
N=9893
0.68
0.62
0.27
0.87
0.42
0.17
0.80
<.0001
<.0001
0.023
P-value
294 (19)
89 (25)
1517 (21)
111 (20)
56 (23)
56 (23)
202 (27)
66 (25)
1192 (21)
222 (21)
621 (17)
693 (23)
474 (25)
353 (23)
322 (20)
337 (22)
277 (18)
289 (19)
210 (26)
429 (21)
1359 (21)
Yes
N=1788
n (%)
1286 (81)
265 (75)
5827 (79)
438 (80)
192 (77)
192 (77)
558 (73)
194 (75)
4551 (79)
853 (79)
3026 (83)
2342 (77)
1413 (75)
1216 (77)
1256 (80)
1209 (78)
1294 (82)
1213 (80)
593 (73)
1578 (79)
5203 (79)
No
N=6781
n (%)
Hyperopia (+2D)
N=8569
0.02
0.20
0.50
<.0001
0.07
0.74
0.83
<.0001
<.0001
0.52
P-value
Frequency Distributions Of Demographic, Behavioral, Clinical, and Ocular Risk Factors in Children With and Without Myopia and Hyperopia in the
Multi-Ethnic Pediatric Eye Disease Study and the Baltimore Pediatric Eye Disease Study
Table 1
et al.
Page 12
2 (15)
Down syndrome
Yes
N=378
n (%)
Cerebral palsy
848 (88)
1060 (96)
2516 (96)
221 (94)
8831 (96)
4320 (96)
8644 (96)
4361 (96)
122 (98)
540 (97)
18 (86)
11 (85)
No
N=9515
n (%)
<0.0001
0.93
0.39
0.049
0.18
0.83
0.48
0.54
0.18
0.26
0.01
0.03
P-value
234 (27)
237 (23)
548 (23)
44 (22)
1755 (21)
843 (21)
1734 (21)
875 (21)
35 (29)
125 (24)
9 (56)
2 (17)
Yes
N=1788
n (%)
623 (73)
773 (77)
1877 (77)
160 (78)
6655 (79)
3254 (79)
6493 (79)
3348 (79)
86 (71)
388 (76)
7 (44)
10 (83)
No
N=6781
n (%)
Hyperopia (+2D)
N=8569
<0.0001
0.28
0.01
0.80
0.06
0.57
0.02
0.52
0.03
0.04
<0.01
0.72
P-value
et al.
Page 13
et al.
Page 14
Table 2
Multivariable Logistic Regression Analysis of Risk Factors for Myopia (-1D) in the Multi-Ethnic Pediatric
Eye Disease Study and the Baltimore Pediatric Eye Disease Study
Order of Entry into
Model
OR
Astigmatism >=1.5D
4.37
3.45
5.54
Race
2
6.01
3.95
9.14
3.23
2.03
5.11
95% CI
2.04
1.37
3.06
2.16
1.51
3.09
1.71
1.19
2.47
1.11
0.74
1.66
0.96
0.64
1.45
1.50
1.17
1.93
et al.
Page 15
Table 3
Multivariable Logistic Regression Analysis of Risk Factors for Hyperopia (+2D) in the Multi-Ethnic
Pediatric Eye Disease Study and the Baltimore Pediatric Eye Disease Study
Order of Entry
into Model
Race
OR
95% CI
1.63
1.43
1.87
1.49
1.32
1.68
1.43
1.21
1.69
1.44
1.21
1.72
Astigmatism >=1.5D
Yes vs. No
Age
1.44
0.94
1.40
0.81
0.68
0.97
0.74
0.62
0.88
0.95
0.80
1.13
0.89
0.75
1.05
1.51
1.12
1.69